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Goliath Catfish Spawning in the Far Western Amazon Confirmed by the Distribution of Mature Adults, Drifting Larvae and Migrating Juveniles

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Goliath Catfish Spawning in the Far Western Amazon Confirmed by the Distribution of Mature Adults, Drifting Larvae and Migrating Juveniles www.nature.com/scientificreports OPEN Goliath catfish spawning in the far western Amazon confirmed by the distribution of mature adults, Received: 28 June 2016 Accepted: 28 December 2016 drifting larvae and migrating Published: 06 February 2017 juveniles Ronaldo B. Barthem1, Michael Goulding2, Rosseval G. Leite3, Carlos Cañas2, Bruce Forsberg3, Eduardo Venticinque4, Paulo Petry5, Mauro L. de B. Ribeiro6, Junior Chuctaya7 & Armando Mercado2 We mapped the inferred long-distance migrations of four species of Amazonian goliath catfishes (Brachyplatystoma rousseauxii, B. platynemum, B. juruense and B. vaillantii) based on the presence of individuals with mature gonads and conducted statistical analysis of the expected long-distance downstream migrations of their larvae and juveniles. By linking the distribution of larval, juvenile and mature adult size classes across the Amazon, the results showed: (i) that the main spawning regions of these goliath catfish species are in the western Amazon; (ii) at least three species—B. rousseauxii, B. platynemum, and B. juruense—spawn partially or mainly as far upstream as the Andes; (iii) the main spawning area of B. rousseauxii is in or near the Andes; and (iv) the life history migration distances of B. rousseauxii are the longest strictly freshwater fish migrations in the world. These results provide an empirical baseline for tagging experiments, life histories extrapolated from otolith microchemistry interpretations and other methods to establish goliath catfish migratory routes, their seasonal timing and possible return (homing) to western headwater tributaries where they were born. The Amazon has two main groups of migratory fish species, and they belong to the orders Siluriformes (catfishes) and Characiformes (characins)1–3. Major fisheries in the Amazon are based on knowledge of the seasonal upstream and downstream movements of fish, although the life cycles are poorly known by fishermen because the species enter and leave local fishing areas4–6. Long-distance fish migrations (> 1,000 km) that exclusively or partially involve freshwater are known for salmon7 and eels8 but have also been inferred for Amazon goliath catfishes of the family Pimelodidae9–12. Although the migrations of most catfish species are poorly known, the general pattern reported is upstream movement to spawn, downstream passive drifting and even active migra- tion of young juveniles to enter nursery habitats in river channels, floodplains or estuaries7,13–15. In the Amazon, goliath catfishes are major river channel and estuarine predators that are represented by a paraphyletic group of six extant and one fossil species of the genus Brachyplatystoma16–18 with a maximum known adult fork length (FL) of 60–280 cm9 (Fig. 1). 1Museu Paraense Emilio Goeldi (Belém, Pará, Brazil), Caixa Postal 399, Belém, 66040-170, PA, Brazil. 2Wildlife Conservation Society (WCS), 2300 Southern Boulevard, Bronx, 10460, New York, USA. 3Instituto Nacional de Pesquisas da Amazônia (INPA) Cx Postal 478, Manaus, AM, 69011-970, Brazil. 4Universidade Federal do Rio Grande do Norte (UFRN), Depto. de Ecologia, 59072-970 - Natal, RN – Brazil. 5The Nature Conservancy (TNC), 4245 Fairfax Drive, Arlington, VA, 22203 & Museum of Comparative Zoology, Harvard University, MA, Cambridge, USA. 6Instituto Brasileiro de Geografia e Estatística (IBGE), Reserva Ecológica do IBGE, DF 001, KM 38 - C.P. 8588, Brasília, Brazil. 7Universidade Federal do Rio Grande do Sul, Post-graduate Programme of Animal Biology, Laboratório de Ictiologia Departamento de Zoologia - UFRGS Av. Bento Gonçalves, 9500 - Bloco IV - Prédio 43435 CEP 91509-900 - Porto Alegre - RS – Brazil. Correspondence and requests for materials should be addressed to R.B.B. (email: barthem@ superig.com.br) or M.G. (email: [email protected]) SCIENTIFIC REPORTS | 7:41784 | DOI: 10.1038/srep41784 1 www.nature.com/scientificreports/ Figure 1. Migratory goliath catfishes (Brachyplatystoma, Pimelodidae). (A) B. vaillantii (piramutaba in Portuguese, pirabutón in Spanish); (B) B. rousseauxii (dourada in Portuguese, dorado in Spanish); (C) B. platynemum (babão in Portuguese, mota flemosa in Spanish); (D) B. juruense (zebra in Portuguese, zebra in Spanish); (E) Dorado migrations exploited by fishermen. The Santo Antônio Dam on the Madeira River now drowns the Teotônio Rapids (shown here) where B. rousseauxii (species in photo) and B. platynemum were previously exploited and easily detected when migrating. Photos by M. Goulding. The first hypotheses of goliath catfish migration focused on B. rousseauxii and B. vaillantii, the most impor- tant commercial species, and their dependence on the Amazon River estuary as their nursery and inland rivers as feeding and spawning areas9. The spawning areas, however, were only identified as being located in the west- ern Amazon, a vast region of at least 2 million km2 that includes parts of Colombia, Ecuador, Peru, Bolivia and Brazil. More recent biological studies based on commercial fisheries in all major western Andes-Amazon trib- utary basins19–23 established the seasonal, and in some cases year-round, presence of mature goliath catfishes in the western Amazon to at least a few hundred km downstream of the Andes. However, these investigations could not verify the spawning areas, leaving the possibility that they are located farther upriver and closer to the Andes. We present data on the distribution of goliath catfish (Brachyplatystoma) adults, larvae and juveniles across the Amazon Basin, including areas in or near the Andes. Even without tagging experiments, the general differ- ential distribution of sub-adult (downstream) and adult (upstream) goliath catfish size-classes9, as well as otolith microchemistry data10, strongly indicates that long-distance upstream goliath catfish migration occurs. Seasonal upstream goliath catfish movements are also visually obvious at some cataracts, such as those of the Madeira River (Fig. 1) in Brazil, before dams were built4, and those of the Caquetá River in Colombia6. Therefore, it is reasonable to hypothesize that long-distance downstream migrations of young fish occurs, otherwise there would be no recruitment to nurseries, in some cases as far downstream as the Amazon River estuary. To test the goliath catfish migratory hypothesis related to western spawning regions, we mapped the presence of mature adults complemented by the seasonal and geographical variation in abundance and length of larvae and juveniles in river channels across the Amazon, including in the estuary. Two complementary geographical and temporal perspectives were used. The first focused on the Madeira Basin, the Amazon’s largest sub-basin with headwaters in the Andes, and where year-round collections were performed. The second included most of the Amazon and available data from all years. Our study shows that spawning for at least B. rousseauxii, B. juruense and B. platynemum occurs in or near the Andes and demonstrates conclusively that long-distance down- stream migration of their larvae and juveniles occurs. The great variation in B. platynemum larvae size across the Amazon indicates a much wider nursery area than just the Andean region. Size-class data for B. vaillantii indicate long-distance migration and spawning in the western Amazon but do not confirm it near the Andes. Our results are also discussed in light of published goliath life history hypotheses derived from genetic and otolith isotope signatures. Results Adult Distribution and Gonadal Stage. Fish length and gonadal data derived from specimens cap- tured in fisheries in major Andes-Amazon sub-basins in Brazil, Bolivia and Peru, complemented by published data from studies based in Colombia19,23 and Ecuador24, show the wide distribution of mature B. rousseauxii, B. platynemum and B. juruense in all major turbid rivers with headwaters in the Andes, including the Amazon River main channel (Fig. 2 and Table 1). Mature fish are defined as ripe individuals, that is, individuals with fully devel- oped ova or testes25. Brachyplatystoma rousseauxii has the widest distribution. In addition to whitewater (turbid) rivers arising in the Andes, it is found in many clearwater and blackwater tributaries that arise on the Brazilian and Guiana Shields. With the exception of the lower Tocantins River26, which is part of the Amazon River estuary, B. rousseauxii is rarely registered in the fisheries of blackwater and clearwater rivers, an indication of its rarity in these drainages. The only Brazilian or Guiana shield rivers where mature long-distance migratory goliath catfishes SCIENTIFIC REPORTS | 7:41784 | DOI: 10.1038/srep41784 2 www.nature.com/scientificreports/ Figure 2. Distribution of sites investigated and locations of mature goliath catfishes. (a) Sites investigated by the authors and others from published data. (b–e) Locations of mature goliath catfishes by species. Figure was created by authors with ArcGIS for Desktop Advanced 10.2, MapPublisher 9.6 tool inside Adobe Illustrator CC, and Adobe Illustrator CC, 2.0. were found was the Branco, a semi-turbid tributary of the Negro River. Of the goliath species considered, only B. rousseauxii was present in the Branco River, but it is of minimal importance in fisheries there and is reported by fishermen to be relatively rare. In contrast to the other three widely distributed species discussed in this paper, B. vaillantii is rare or naturally absent above the Madeira Rapids in the southwestern Amazon of Bolivia and Peru. The new fishways around the Madeira dams,
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